Emergent neutrality in consumer-resource dynamics

D’Andrea, Rafael; Gibbs, Theo; O’Dwyer, James P.

doi:10.1101/710541

Cited by 4 publications

(5 citation statements)

References 54 publications

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“…Intriguingly, the abundance distributions of all five of our gut bacterial species, when inoculated together, are similar to one another. The average Shannon entropy of the five-species community (H ϭ 1.16 Ϯ 0.24) (see Text S1 in the supplemental material) also resembles that of a purely neutrally assembled community (H ϭ 1.61), reminiscent of dynamics mimicking neutral assembly that emerge from multispecies dynamics driven by resource use constraints (48,75).…”

Section: Discussionmentioning

confidence: 93%

Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome

Sundarraman

Hay

et al. 2020

mBio

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The microbial communities resident in animal intestines are composed of multiple species that together play important roles in host development, health, and disease. Due to the complexity of these communities and the difficulty of characterizing them in situ, the determinants of microbial composition remain largely unknown. Further, it is unclear for many multispecies consortia whether their species-level makeup can be predicted based on an understanding of pairwise species interactions or whether higher-order interactions are needed to explain emergent compositions. To address this, we examine commensal intestinal microbes in larval zebrafish, initially raised germfree, to allow the introduction of controlled combinations of bacterial species. Using a dissection and plating assay, we demonstrate the construction of communities of one to five bacterial species and show that the outcomes from the two-species competitions fail to predict species abundances in more complex communities. With multiple species present, interbacterial interactions become weaker, suggesting that higher-order interactions in the vertebrate gut stabilize complex communities. IMPORTANCE Understanding the rules governing the composition of the diverse microbial communities that reside in the vertebrate gut environment will enhance our ability to manipulate such communities for therapeutic ends. Synthetic microbial communities, assembled from specific combinations of microbial species in germfree animals, allow investigation of the fundamental question of whether multispecies community composition can be predicted solely based on the combined effects of interactions between pairs of species. If so, such predictability would enable the construction of communities with desired species from the bottom up. If not, the apparent higher-order interactions imply that emergent community-level characteristics are crucial. Our findings using up to five coexisting native bacterial species in larval zebrafish, a model vertebrate, provide experimental evidence for higher-order interactions and, moreover, show that these interactions promote the coexistence of microbial species in the gut.

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Section: Discussionmentioning

confidence: 93%

Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome

Sundarraman

Hay

et al. 2020

mBio

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“…Such probabilistic events can be simulated within the framework of consumer-resource models [ 89 , 90 , 98 ]. Similarly, demographic noise can be incorporated [ 100 ], capturing the emergence of apparent neutrality, i.e., giving all community members the appearance of being ecologically equivalent. Adaptation of the model to include environmental fluctuations revealed a U-shaped relationship between community diversity and disturbance intensity, which a Lotka-Volterra model failed to capture [ 101 ].…”

Section: Ecological Modelsmentioning

confidence: 99%

Ecological modelling approaches for predicting emergent properties in microbial communities

et al. 2022

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Recent studies have brought forward the critical role of emergent properties in shaping microbial communities and the ecosystems they are part of. Emergent properties - patterns or functions that cannot be deduced linearly from the properties of the constituent parts - underlie important ecological characteristics such as resilience, niche expansion, and spatial self-organisation. While it is clear that emergent properties are a consequence of interactions within the community, their non-linear nature makes mathematical modelling imperative for establishing the quantitative link between community structure and function. As the need for conservation and rational modulation of microbial ecosystems is increasingly apparent, so is the consideration of the benefits and limitations of the approaches to model emergent properties. Here we review ecosystem modelling approaches from the viewpoint of emergent properties. We consider the scope, advantages, and limitations of Lotka-Volterra, consumer-resource, trait-based, individual-based, and genome-scale metabolic models. Future efforts in this research area would benefit from capitalising on the complementarity between these approaches towards enabling rational modulation of complex microbial ecosystems.

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“…Such large-scale coexistence can also emerge 387 naturally from contemporary resource competition models [46,75], in which 388 cross-feeding or metabolic tradeoffs necessarily involve multiple interacting species. assembled community (H = 1.61), reminiscent of dynamics mimicking neutral assembly 393 that emerge from multi-species dynamics driven by resource use constraints [46,76]. 394 Our findings imply that measurements of two-species interactions among microbial 395 residents of the vertebrate gut are likely to be insufficient for predictions of community 396 dynamics and composition.…”

mentioning

confidence: 92%

“…In 71 contrast, work using well-defined bacterial assemblies of up to five species in the fruit fly 72 D. melanogaster found strong higher order interactions governing microbe-dependent 73 effects on host traits such as lifespan [32]. 74 To our knowledge, there have been no quantitative assessments of inter-bacterial 75 interactions using controlled combinations of microbial species in a vertebrate host, 76 leaving open the question of whether higher order interactions are strong, or whether 77 pairwise characterizations suffice to predict intestinal community structure. We 78 Dissection and Plating 120…”

Section: Introductionmentioning

confidence: 99%

Quantifying multi-species microbial interactions in the larval zebrafish gut

Sundarraman

et al. 2020

Preprint

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These authors contributed equally to this work. AbstractThe microbial communities resident in animal intestines are composed of multiple species that together play important roles in host development, health and disease. Due to the complexity of these communities and the difficulty of characterizing them in situ, the determinants of microbial composition remain largely unknown. Further, it is unclear for many multi-species consortia whether their species-level makeup can be predicted based on an understanding of pairwise species interactions, or whether higher-order interactions are needed to explain emergent compositions. To address this, we examine commensal intestinal microbes in larval zebrafish, initially raised germ-free to allow introduction of controlled combinations of bacterial species. Using a dissection and plating assay, we demonstrate the construction of communities of one to five bacterial species and show that the outcomes from the two-species competitions fail to predict species abundances in more complex communities. With multiple species present, inter-bacterial interactions become weaker and more cooperative, suggesting that higher-order interactions in the vertebrate gut may stabilize complex communities. 5 immune regulation [5-10] and a wide range of diseases [11][12][13][14][15][16][17][18][19][20]. 6 Despite the importance of intestinal communities, the determinants of their 7 composition remain largely unknown. A growing number of studies map the effects of 8 external perturbations, such as antibiotic drugs [21, 22] and dietary fiber [23] and 9 fat [24, 25] on the relative abundance of gut microbial species. Intrinsic inter-microbial 10interactions, however, are especially challenging to measure and are important not only 11 for shaping community composition in the absence of perturbations but also for 12 propagating species-specific perturbations to the rest of the intestinal ecosystem. 13The considerable majority of studies of the gut microbiota have been performed on 14 naturally assembled microbiomes by sequencing DNA extracted from fecal samples, an 15May 28, 2020 1/23approach that provides information about the microbial species and genes present in the 16 gut, but that imposes several limitations on the inference of inter-species interactions. 17The high diversity of natural intestinal communities, and therefore the low abundance 18 of any given species among the multitude of its fellow residents, implies that stochastic 19 fluctuations in each species' abundance will be large, easily masking true biological 20 interactions. The accuracy of inference is considerably worse if only relative, rather than 21 absolute, abundance data is available [26-29], as is typically the case in 22 sequencing-based studies. Finally, we note that fecal sampling assesses only the 23 microbes that have exited the host, which may not be representative of the intestinal 24 community [30]. 25 An alternative approach to using DNA sequencing and naturally assembled 26 host-microbiota systems is to build suc...

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Emergent neutrality in consumer-resource dynamics

Cited by 4 publications

References 54 publications

Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome

Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome

Ecological modelling approaches for predicting emergent properties in microbial communities

Quantifying multi-species microbial interactions in the larval zebrafish gut

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